Abstract
Main conclusion
Identification of PbLTP genes in pear and functional characterization of PbLTP4 in the transport of suberin monomers of russet skin formation.
Abstract
Non-specific lipid-transfer protein (nsLTP) is an abundant and diverse alkaline small molecule protein in the plant kingdom with complex and diverse biophysiological functions, such as transfer of phospholipids, reproductive development, pathogen defence and abiotic stress response. Up to now, only a tiny fraction of nsLTPs have been functionally identified, and the distribution of nsLTPs in pear (Pyrus bretschneideri) (PbLTPs) has not been fully characterized. In this study, the genome-wide analysis of the nsLTP gene family in the pear genome identified 67 PbLTP proteins, which could be divided into six types (1, 2, C, D, E, and G). Similar intron/exon structural patterns were observed in the same type, strongly supporting their close evolutionary relationship. In addition, PbLTP4 was highly expressed in russet pear skin compared with green skin, which was located in the plasma membrane. Coexpression network analysis showed that PbLTP4 closely related to suberin biosynthetic genes. The biological function of PbLTP4 in promoting suberification has been demonstrated by overexpression in Arabidopsis. Identification of suberin monomers showed that PbLTP4 promotes suberification by regulating 9,12-octadecadienoic acid and hexadecanoic acid transport. These results provide helpful insights into the characteristics of PbLTP genes and their biological function in the transport of suberin monomers of russet skin formation.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The transcriptome data sets supporting the conclusions of this article are available in the National Center for Biotechnology Information (https://dataview.ncbi.nlm.nih.gov/object/PRJNA908284).nta.
Abbreviations
- DAFB:
-
Days after full bloom
- LTPG:
-
Glycosylphosphatidylinositol (GPI)-anchored LTP
- nsLTP:
-
Non-specific lipid-transfer protein
References
Armstrong RA, Eperjesi F, Gilmartin B (2002) The application of analysis of variance (ANOVA) to different experimental designs in optometry. Ophthalmic Physiol Opt 22(3):248–256. https://doi.org/10.1046/j.1475-1313.2002.00020.x
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335
Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genom 9:86. https://doi.org/10.1186/1471-2164-9-86
D’Agostino N, Buonanno M, Ayoub J, Barone A, Monti SM, Rigano MM (2019) Identification of non-specific Lipid Transfer Protein gene family members in Solanum lycopersicum and insights into the features of Sola l 3 protein. Sci Rep 9(1):1607. https://doi.org/10.1038/s41598-018-38301-z
Debono A, Yeats TH, Rose JK, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21(4):1230–1238. https://doi.org/10.1105/tpc.108.064451
Edstam MM, Edqvist J (2014) Involvement of GPI-anchored lipid transfer proteins in the development of seed coats and pollen in Arabidopsis thaliana. Physiol Plant 152(1):32–42. https://doi.org/10.1111/ppl.12156
Edstam MM, Blomqvist K, Eklöf A, Wennergren U, Edqvist J (2013) Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin. Plant Mol Biol 83(6):625–649. https://doi.org/10.1007/s11103-013-0113-5
Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR (2015) HMMER web server: 2015 update. Nucleic Acids Res 43(W1):W30–W38. https://doi.org/10.1093/nar/gkv397
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Hereditas 29(8):1023–1026
Heng W, Wang Z, Jiang X, Jia B, Liu P, Liu L, Ye Z, Zhu L (2016) The role of polyamines during exocarp formation in a russet mutant of “Dangshansuli” pear (Pyrus bretschneideri Rehd.). Plant Cell Rep 35(9):1841–1852. https://doi.org/10.1007/s00299-016-1998-7
Heng W, Huang H, Li F, Hou Z, Zhu L (2017) Comparative analysis of the structure, suberin and wax composition and key gene expression in the epidermis of ‘Dangshansuli’ pear and its russet mutant. Acta Physiol Plant 39(7):150. https://doi.org/10.1007/s11738-017-2443-4
Hou Z, Jia B, Li F, Liu P, Liu L, Ye Z, Zhu L, Wang Q, Heng W (2018) Characterization and expression of the ABC family (G group) in “Dangshansuli” pear (Pyrus bretschneideri Rehd.) and its russet mutant. Genet Mol Biol 41(1):137–144. https://doi.org/10.1590/1678-4685-gmb-2017-0109
Ji J, Lv H, Yang L, Fang Z, Zhuang M, Zhang Y, Liu Y, Li Z (2018) Genome-wide identification and characterization of non-specific lipid transfer proteins in cabbage. PeerJ 6:e5379. https://doi.org/10.7717/peerj.5379
Kristensen AK, Brunstedt J, Nielsen KK, Roepstorff P, Mikkelsen JD (2000) Characterization of a new antifungal non-specific lipid transfer protein (nsLTP) from sugar beet leaves. Plant Sci 155(1):31–40. https://doi.org/10.1016/s0168-9452(00)00190-4
Li G, Hou M, Liu Y, Pei Y, Ye M, Zhou Y, Huang C, Zhao Y, Ma H (2019) Genome-wide identification, characterization and expression analysis of the non-specific lipid transfer proteins in potato. BMC Genom 20(1):375. https://doi.org/10.1186/s12864-019-5698-x
Liu F, Lu CM (2013) An overview of non-specific lipid transfer protein in plant. Hereditas 35(3):307–314. https://doi.org/10.3724/sp.j.1005.2013.00307
Liu F, Zhang X, Lu C, Zeng X, Li Y, Fu D, Wu G (2015) Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. J Exp Bot 66(19):5663–5681. https://doi.org/10.1093/jxb/erv313
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Ma H, Zhao J (2010) Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). J Exp Bot 61(10):2647–2668. https://doi.org/10.1093/jxb/erq104
Missaoui K, Gonzalez-Klein Z, Pazos-Castro D, Hernandez-Ramirez G, Garrido-Arandia M, Brini F, Diaz-Perales A, Tome-Amat J (2022) Plant non-specific lipid transfer proteins: an overview. Plant Physiol Biochem 171:115–127. https://doi.org/10.1016/j.plaphy.2021.12.026
Molina A, Segura A, García-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316(2):119–122. https://doi.org/10.1016/0014-5793(93)81198-9
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300
Nomberg G, Marinov O, Arya GC, Manasherova E, Cohen H (2022) The key enzymes in the suberin biosynthetic pathway in plants: an ipdate. Plants 11(3):392. https://doi.org/10.3390/plants11030392
Salminen TA, Blomqvist K, Edqvist J (2016) Lipid transfer proteins: classification, nomenclature, structure, and function. Planta 244(5):971–997. https://doi.org/10.1007/s00425-016-2585-4
Scheurer S, Schülke S (2018) Interaction of non-specific lipid-transfer proteins with plant-derived lipids and its impact on allergic sensitization. Front Immunol 9:1389. https://doi.org/10.3389/fimmu.2018.01389
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
Vishwanath SJ, Delude C, Domergue F, Rowland O (2015) Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep 34(4):573–586. https://doi.org/10.1007/s00299-014-1727-z
Wang C, Chen L, Yang H, Yang S, Wang J (2019) Genome-wide identification, expression and functional analysis of Populus xylogen-like genes. Plant Sci 287:110191. https://doi.org/10.1016/j.plantsci.2019.110191
Wang X, Li Q, Cheng C, Zhang K, Lou Q, Li J, Chen J (2020) Genome-wide analysis of a putative lipid transfer protein LTP_2 gene family reveals CsLTP_2 genes involved in response of cucumber against root-knot nematode (Meloidogyne incognita). Genome 63(4):225–238. https://doi.org/10.1139/gen-2019-0157
Wang Q, Liu Y, Wu X, Wang L, Li J, Wan M, Jia B, Ye Z, Liu L, Tang X, Tao S, Zhu L, Heng W (2022) MYB1R1 and MYC2 regulate ω-3 fatty acid desaturase involved in ABA-mediated suberization in the russet skin of a mutant of “Dangshansuli” (Pyrus bretschneideri Rehd.). Front Plant Sci 13:910938. https://doi.org/10.3389/fpls.2022.910938
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191. https://doi.org/10.1093/bioinformatics/btp033
Wei K, Zhong X (2014) Non-specific lipid transfer proteins in maize. BMC Plant Biol 14:281. https://doi.org/10.1186/s12870-014-0281-8
Yang Y, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22(6):543–551. https://doi.org/10.1046/j.1365-313x.2000.00760.x
Yap CK, Eisenhaber B, Eisenhaber F, Wong WC (2016) xHMMER3x2: Utilizing HMMER3’s speed and HMMER2’s sensitivity and specificity in the glocal alignment mode for improved large-scale protein domain annotation. Biol Direct 11(1):63. https://doi.org/10.1186/s13062-016-0163-0
Zhang Q, Xie Z, Zhang R, Xu P, Liu H, Yang H, Doblin MS, Bacic A, Li L (2018) Blue light regulates secondary cell wall thickening via MYC2/MYC4 activation of the NST1-directed transcriptional network in Arabidopsis. Plant Cell 30(10):2512–2528. https://doi.org/10.1105/tpc.18.00315
Funding
This project was supported by the National Natural Science Foundation of China (31972985), the China Agriculture Research System (CARS-28), and Anhui Province Fruit-Tree Industry Technology System (AHCYTX-10).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
425_2023_4153_MOESM2_ESM.tif
Supplementary file2 Phylogenetic analysis of nsLTPs from pear and Arabidopsis thaliana. The tree was constructed with IQ-TREE v.1.6 software. The nsLTPs clustered into 6 distinct clades, marked by curves of different colors (TIF 2447 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, J., Wang, Q., Wang, Y. et al. Identification of nsLTP family in Chinese white pear (Pyrus bretschneideri) reveals its potential roles in russet skin formation. Planta 257, 113 (2023). https://doi.org/10.1007/s00425-023-04153-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04153-9